©2017 Institute of Parasitology, SAS, Košice DOI 10.1515/helm-2017-0038

HELMINTHOLOGIA, 54, 4: 314 – 321, 2017

New data on helminth fauna of of prey (Falconiformes, Accipitriformes, Strigiformes) in the Slovak Republic

P. KOMOROVÁ1*, J. SITKO2, M. ŠPAKULOVÁ3, Z. HURNÍKOVÁ3,1, R. SAŁAMATIN4, 5, G. CHOVANCOVÁ6

1Department of Epizootology and Parasitology, Institute of Parasitology, The University of Veterinary Medicine and Pharmacy in Košice, Komenského 73, 041 81 Košice, Slovak Republic, *E-mail: [email protected]; 2Ornitological Station of Commenius Museum in Přerov, Bezručova 10, 750 02 Přerov, Czech Republic; 3Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic; 4Department of General Biology and Parasitology, Medical University of Warsaw, Chałubińskiego 5, 02-004 Warsaw, Poland; 5Department of Parasitology, National Institute of Public Health – National Institute of Hygiene, Chocimska 24, 00-719 Warsaw, Poland; 6Research Station and Museum of the Tatra National Park, 059 60 Tatranská Lomnica, Slovak Republic

Article info Summary

Received December 1, 2016 In the years 2012-2014, carcasses of 286 birds of prey from the territory of Slovakia were examined Accepted July 4, 2017 for the presence of helminth parasites. The number of in the study was 23; fi ve belonging to the Falconiformes order, eleven to Accipitriformes, and seven to Strigiformes. A fi nding of Cestoda class comprehended 4 families: Paruterinidae (4), Dilepididae (2), Mesocestoididae (2) and Anoplo- cephalidae (1). Birds of prey were infected with 6 families Nematoda species of the class: Syngamidae (1), Habronematidae (2), Tetrameridae (3), Physalopteridae (1), Acuariidae (1), and Anisakidae (2). Out of the Adenophorea class, the Capillariidae family (1) was confi rmed. The group was represented by the Paleacanthocephala class, the Centrorhynchidae family (3). Out of the class, 12 different species of fl ukes were found, belonging to the Diplostomidae (5), Cyathocotylidae (1), Strigeidae (4), Opistorchidae (1), and Plagiorchidae (1) fami- lies. The most frequent helminth species infecting diurnal birds of prey was Strigea falconis. This fl uke was confi rmed in one bird species from the Falconiformes order and in eight species from the Accipitriformes order. In nocturnal birds of prey, the most common fi nding was the acanthocephalan Centrorhynchus aluconis, identifi ed in four different host species of the Strigiformes order. In total, 23 helminth species were recorded for the fi rst time in Slovakia. Keywords: helminth parasites; infection; nocturnal and diurnal birds of prey

Introduction Sanmartín et al. (2004), Illescas Gomez et al. (1993), and Santoro et al. (2012a, b). Birds of prey are predatory residing at the top of a food Forty-three different species of birds of prey, belonging to the Fal- chain and they usually get infected with parasites via ingestion of coniformes, Accipitriformes, and Strigiformes orders, nest or occur prey, thus serving as intermediate hosts of many parasite species. in Slovakia territory (Kovalik et al., 2010). The most abundant spe- Types and diversity of the prey preferred by individual species rep- cies is the (Buteo buteo) that nests in different resent one of the factors affecting the parasite diversity in those forest biotopes, but it is very well adapted also to the agricultural hosts. land. However in low quantities, on the territory of Slovakia we can Since majority of birds of prey species in Europe are protected, the also fi nd the species that are very sensitive to the environmental research and knowledge of the parasite fauna is only fragmentary. changes associated with anthropogenic impacts (Circus pygargus, Comprehensive research projects studying all helminth groups in Milvus milvus) (Krivjanský, 2009). birds of prey were accomplished by the Borgsteede et al. (2003), In Slovakia, only two research papers, aimed at parasites in birds

* – corresponding author

314 of prey, have been published in the 20th century. Tenora & Lusk minths, 17 out of 85 diurnal birds of prey from the Falconiformes or- (1960) and Škarda (1964) studied the helminth fauna of birds in der were infected (20 %), and the parasitic infection was confi rmed Czechoslovakia and published several fi ndings in birds of prey in 114 out of 156 birds from the Accipitriformes order (73.1 %). In from the Slovak part of the country. For a subsequent period of 50 nocturnal birds of prey (Strigiformes order), helminths were found years, at the times of dynamic climate changes, no comprehen- in 28 out of 45 individuals (62.2 %). sive research of this host group has been carried out. Recently, A total of 33 helminth taxa were registered. In the Falconiformes two papers on fl ukes and thorny-headed worms were published order, 9 different helminth taxa were determined – 2 Trematoda, 1 (Komorová et al., 2015; Komorová et al., 2016). Cestoda, 4 Secernentea, and 1 Paleacanthocephala. In birds from The aim of our study was to obtain the complex knowledge about the Accipitriformes order, in total 27 helminth species were found the current status of the parasite fauna in birds of prey in Slovakia. – 9 Trematoda, 6 Cestoda, 1 Adenophorea, 8 Secernentea, and 3 Paleacanthocephala. In nocturnal birds of prey (Strigiformes) 10 Material and Methods helminth species were detected – 2 Trematoda, 2 Cestoda, 1 Ad- enophorea, 4 Secernentea, and 1 Paleacanthocephala (Table 1). During the period of 2012 – 2014, 286 carcasses of birds of prey The information on parasite species, names and numbers of in- belonging to 23 species of the Falconiformes, Accipitriformes, and fected hosts (NIH), prevalence (P in %), intensity of infection (II), Strigiformes orders were examined for the presence of helminths mean intensity (MI), and site of infection is summarized below. (Table 1). The research was conducted upon the permission is- sued by the Ministry of Environment of the Slovak Republic No. Platyhelminthes 6467/2012-2.26467/2012-2.2. The samples were collected from Trematoda various locations of Slovakia in cooperation with departments Diplostomidae Poirier, 1886 of the State Nature Conservancy of the Slovak Republic – The Conodiplostomum perlatum (Ciurea, 1911) Slovenský Kras National Park, The Slovenský Raj National Park, Host: H. albicilla (NIH=1; P=100 %; II=43) – fi rst record in Slovakia The Pieniny National Park, The Regional Conservation Centre in Site of infection: small intestine Prešov, and The Vihorlat Protected Area, as well as with the Mu- seum of the Tatra National Park, the Clinic for Birds and Exotic Conodiplostomum spathula (Creplin, 1829) Animals at the University of Veterinary Medicine and Pharmacy Host: A. heliaca (NIH=1; P=16.7 %; II=13) – fi rst record in Slovakia in Košice, The Raptor Protection of Slovakia, The Rehabilitation Site of infection: small intestine Station in The ZOO Bojnice, and The Košice Airport. Collected bird carcasses were frozen and subjected to helminthological necrop- Neodiplostomum attenuatum (Linstow, 1906) sy. After de-freezing, all organ systems and body cavities were Host: B. buteo (NIH=29; P=24.4 %; II=1-224; MI=25), B. lagopus examined for the presence of parasites. Collected helminths were (NIH=1; P=20 %; II=70), B. rufi nus (NIH=2; P=50 %; II=6-10; washed in distilled water and preserved in 70 % ethanol. For mor- MI=8), P. apivorus (NIH=1; P=100 %; II=3) – fi rst records in Slo- phological identifi cation, the species belonging to the Trematoda vakia and Cestoda classes were stained with iron acetocarmine (Geor- Site of infection: small intestine giev et al, 1986). Lightening of specimens from the Adenopoho- rea, Secernentea, and Paleacanthocephala classes was carried Neodiplostomum canaliculatum (Nicoll, 1914) out using glycerine or lactophenol. The species identifi cation was Host: B. bubo (NIH=1; P=50 %; II=1), S. uralensis (NIH=5; conducted according to Dubois (1968, 1970), Gibson et al. (2002), P=33.3 %; II=5-23; MI=14) – fi rst records in Slovakia Sitko (1998, 2001), and Bray et al. (2008) for Trematoda; Joyeux Site of infection: small intestine & Timon-David (1934), Joyeux & Baer (1936), Rausch (1948), and Khalil et al. (1994) for Cestoda; Hartwich (1975), Baruš et al. Neodiplostomum spathoides Dubois, 1937 (1978), and Gibbons (2010) for Adenophorea; and Secernentea Host: B. rufi nus (NIH=1; P=25 %; II=4), C. aeruginosus (NIH=2; and Meyer (1933), Petrochenko (1958), Dimitrova et al. (1997), P=50 %; II=8-15; MI=11.5) – fi rst records in Slovakia and Dimitrova & Gibson (2005) for Paleacanthocephala. Ecologi- Site of infection: small intestine cal parameters (prevalence, mean intensity, diversity) were evalu- ated according to Bush et al. (2007). Cyathocotylidae Mühling, 1898 The voucher specimens are deposited in the collection of The In- Paracoenogonimus ovatus Katsurada, 1914 stitute of Parasitology at the SAS in Košice. Host: H. albicilla (NIH=1; P=100 %; II=1) – fi rst record in Slovakia Site of infection: small intestine Results Strigeidae Railiet, 1919 Out of 286 examined birds, 156 (54.5 %) were infected with hel- fl exilis (Dubois, 1934)

315 Table 1. List of birds of prey species investigated and nubmers of hosts infected with individual parasite classes.

Order/bird species No. of birds parasitized by:

No. of examined/ parasitized birds Tremtoda Cestoda Secernentea Adenophorea Paleacanthocephala

Falconiformes 85/15 3 3 8 0 2 Falco cherrug Gray, 1834 3/2 - - 2 - - Falco columbarius L., 1758 1 - - - - - Falco peregrinus Tunstall, 1771 5 - - - - - Falco subbuteo L., 1758 3/3 1 - 3 - - Falco tinnunculus L., 1758 73/10 2 3 3 - 2 Accipitriformes 156/114 63 51 55 19 13 Accipiter gentilis L., 1758 5/3 2 1 1 - - Accipiter nisus L., 1758 9/5 1 - 4 1 - Aquila heliaca Savigny, 1809 6/4 1 2 2 1 - Buteo buteo (L., 1758) 119/89 48 44 41 16 12 Buteo lagopus (Pontoppidan, 1763) 5/4 2 - 4 1 - Buteo rufi nus (Cretzschmar, 1829) 4/3 3 2 2 - 1 Circus aeruginosus (L., 1758) 4/3 3 1 1 - - Circus pygargus (L., 1758) 1 - - - - - Haliaeetus albicilla (L., 1758) 1/1 1 - - - - Milvus milvus (L., 1758) 1/1 1 - - - - Pernis apivorus (L., 1758) 1/1 1 1 - - - Strigiformes 45/28 10 6 5 17 19 Asio otus (L., 1758) 13/7 2 - - 6 1 Athene noctua (Scopoli, 1769) 1 - - - - - Bubo bubo (L., 1758) 2/2 2 - - 1 - Glaucidium passerinum (L., 1758) 1 - - - - - Strix aluco L., 1758 10/3 - 1 - 1 2 Strix uralensis Pallas, 1771 15/15 6 5 5 9 15 Tyto alba (Scopoli, 1769) 3/1 - - - - 1

316 Host: B. rufi nus (NIH=1; P=25 %; II=1), C. aeruginosus (NIH=2; Site of infection: small intestine P=50%; II=1-2; MI=1.5) – fi rst records in Slovakia Paruterina candelabraria (Goeze, 1782) Site of infection: small intestine Host: S. aluco (NIH=1; P=10 %; II=4), S. uralensis (NIH=4; P=26.7 %; II=1-8; MI=3.25) – fi rst records in Slovakia Strigea falconis Szidat, 1928 Site of infection: small intestine Host: F. tinnunculus (NIH=2; P=2.7 %; II=2; MI=2), A. gentilis (NIH=2; P=40 %; II=1-3; MI=2), A. nisus (NIH=1; P=11.1 %; II=3), Dilepididae Railliet et Henry, 1909 A. heliaca (NIH=1; P=16.7 %; II=15), B. buteo (NIH=42; P=35.3 %; Choanotaenia strigium Joyeux & Timon-David, 1934 II=1-575; MI=35.4), B. lagopus (NIH=2; P=40 %; II=5-10; MI=7.5), Host: S. uralensis (NIH=1; P=6.7 %; II=4) – fi rst record in Slovakia B. rufi nus (NIH=3; P=75 %; II=4-18; MI=10.7), C. aeruginosus Site of infection: small intestine (NIH=3; P=75 %; II=1-8; MI=4), M. milvus (NIH=1; P=100 %; II=2) – new host records in Slovakia except for B. buteo Spiniglans trapezoides (Fuhrmann, 1906) Salamatin, 2000 Site of infection: small intestine Host: P. apivorus (NIH=1; P=100 %; II=1) – fi rst record in Slovakia Site of infection: small intestine Strigea strigis Schrank, 1788 Host: A. otus (NIH=2; P=15.4 %; II=2-4; MI=3), B. bubo (NIH=1; Mesocestoididae Perrier, 1897 P=50 %; II=2), S. uralensis (NIH=2; P=13.3 %; II=6-17; MI=11.5) – Mesocestoides perlatus (Goeze, 1782) fi rst records in Slovakia Host: A. gentilis (NIH=1; P=20 %; II=1) – fi rst record in Slovakia Site of infection: small intestine Site of infection: small intestine

Strigea vandenbrokae Dubois, 1936 Mesocestoides sp. Host: P. apivorus (NIH=1; P=100 %; II=7) – fi rst record in Slovakia Host: B. rufi nus (NIH=1; P=25 %; II=1) Site of infection: small intestine Site of infection: small intestine

Opisthorchiidae Looss, 1899 Anoplocephalidae gen. sp. Metorchis bilis (Braun, 1790) Host: B. buteo (NIH=1; P=0.8 %; II=1) Host: H. albicilla (NIH=1; P=100 %; II=2), B. rufi nus (NIH=1; Site of infection: small intestine P=25 %; II=21) – fi rst records in Slovakia Site of infection: gall bladder Nematoda Secernentea Plagiorchiidae Lühe, 1901 Syngamidae Leiper, 1912 Plagiorchis elegans (Rudolphi, 1802) Cyathostoma americana Chapin, 1925 Host: F. subbuteo (NIH=1; P=33.3 %; II=4) – new host record in Host: B. rufi nus (NIH=1; P=25 %; II=2) – fi rst record in Slovakia Slovakia Site of infection: trachea Site of infection: small intestine Habronematidae (Chitwood et Wehr, 1932) Cestoda Cyrnea leptoptera (Rudolphi, 1819) Paruterinidae Fuhrmann, 1907 Host: F. cherrug (NIH=1; P=33.3 %; II=2), F. subbuteo (NIH=2; Cladotaenia circi Yamaguti, 1935 P=66.7 %; II=7-18; MI=12,5), B. buteo (NIH=11; P=9.2 %; II=1- Host: C. aeruginosus (NIH=1; P=25 %; II=1) – fi rst record in Slo- 12; MI=3.55), C. aeruginosus (NIH=1; P=25 %; II=1), S. uralensis vakia (NIH=1; P=6.7 %; II=5) – new host records in Slovakia except for Site of infection: small intestine B. buteo Site of infection: gizzard Cladotaenia globifera (Batsch, 1786) Host: F. tinnunculus (NIH=3; P=4,1 %; II=1-2; MI=1.33), B. buteo Cyrnea spinosa (Gendre, 1923) (NIH=43; P=36.1 %; II=1-20; MI=4.4), B. rufi nus (NIH=1; P=25 %; Host: F. subbuteo (NIH=1; P=33.3 %; II=13), A. nisus (NIH=1; II=1) – new host records in Slovakia except for B. buteo P=11.1 %; II=6) – new host records in Slovakia Site of infection: small intestine Site of infection: gizzard

Cladotaenia spasskii Kobyshev, 1971 Tetrameridae Travassos, 1914 Host: A. heliaca (NIH=2; P=33.3 %; II=1-4; MI=2.5) – fi rst record Microtetrameres cloacitectus Oshmarin, 1956 in Slovakia Host: F. tinnunculus (NIH=2; P=2.7 %; II=4-6; MI=5), B. buteo

317 (NIH=8; P=6.7 %; II=1-183; MI=32.38) – fi rst records in Slovakia P=16.7 %; II=3), B. buteo (NIH=6; P=5 %; II=1-14; MI=6.67), A. Site of infection: gizzard otus (NIH=1; P=7.7 %; II=2), S. uralensis (NIH=5; P=33.3 %; II=4- 12; MI=8.2) – fi rst records in Slovakia Microtetrameres oshmarini Sobolev, 1963 Site of infection: small intestine Host: S. uralensis (NIH=3; P=20 %; II=3-25; MI=14.67) – fi rst re- cord in Slovakia Acanthocephala Site of infection: gizzard Paleacanthocephala Centrorhynchidae Golvan, 1960 sp. Centrorhynchus aluconis (Muller, 1780) Host: S. uralensis (NIH=1; P=6.7 %; II=1) – fi rst record in Slovakia Host: B. buteo (NIH=1; P=0.8 %; II=5), A. otus (NIH=1; P=7.7 %; Site of infection: gizzard II=5), S. aluco (NIH=2; P=20 %; II=5-10; MI=7.5), S. uralensis (NIH=15; P=100 %; II=2-82; MI=22.4), T. alba (NIH=1; P=33.3 %; Physalopteridae (Railliet, 1893) II=2) – new host records in Slovakia except for B. buteo and S. alata Rudolphi, 1819 aluco Host: A. nisus (NIH=2; P=22.2 %; II=1-7; MI=4) – fi rst record in Site of infection: small intestine Slovakia Site of infection: gizzard Centrorhynchus buteonis (Schrank, 1788) Host: B. buteo (NIH=10; P=9.2 %; II=1-15; MI=6.4), B. rufi nus Acuariidae Railliet, Henry et Sisoff, 1912 (NIH=1; P=25 %; II=39) – fi rst records in Slovakia Synhimantus laticeps (Rudolphi, 1819) Site of infection: small intestine Host: F. tinnunculus (NIH=1; P=1.4 %; II=2), A. heliaca (NIH=1; P=16.7 %; II=3), B. buteo (NIH=1; P=0.8 %; II=2), B. lagopus Centrorhynchus globocaudatus (Zeder, 1800) (NIH=1; P=20 %; II=1), B. rufi nus (NIH=1; P=25 %; II=17) – fi rst Host: F. tinnunculus (NIH=2; P=2.7 %; II=1-2; MI=1.5), B. buteo records in Slovakia (NIH=1; P=0.8 %; II=3), B. rufi nus (NIH=1; P=25 %; II=5) – new Site of infection: oesophagus host records in Slovakia Site of infection: small intestine Anisakidae Railliet et Henry, 1912 Porrocaecum angusticolle (Molin, 1860) Discussion Host: F. cherrug (NIH=1; P=33.2 %; II=134), A. gentilis (NIH=1; P=20 %; II=6), A. nisus (NIH=1; P=11.1 %; II=3), A. heliaca (NIH=1; In Europe, there are only few papers comprehensively studying P=16.7 %; II=1), B. buteo (NIH=24; P=20.2 %; II=1-15; MI=3.63), the helminths in birds of prey. The published studies focused main- B. lagopus (NIH=3; P=60 %; II=1-4; MI=2.33), B. rufi nus (NIH=1; ly on particular groups of birds or certain categories of helminths. P=25 %; II=1), S. uralensis (NIH=4; P=26.7 %; II=1-5; MI=2.75) – Complex surveys involving all three major orders of birds of prey new host records in Slovakia except for B. buteo (omitting passeriform shrikes of the Laniidae family) were conduct- Site of infection: stomach, small intestine ed in the Netherlands (Borgsteede et al., 2003), Spain (Sanmartín et al., 2004; Illescas Gomez et al., 1993), and Italy (Santoro et al., Porrocaecum depressum (Zeder, 1800) 2012a, b). Ferrer et al. (2004) examined the incidence of helminths Host: B. buteo (NIH=8; P=6.7 %; II=1-49; MI=9.63), B. rufi nus only in owls from the territory of Spain. In the Czech Republic, (NIH=1; P=25 %; II=3) – new host record in Slovakia except of Sitko published decades-long scientifi c studies of fl ukes in diurnal B. buteo (1998) and nocturnal raptors (2001). Research from the territory of Site of infection: stomach, small intestine Slovakia was published in the former Czechoslovakia by Ryšavý (1957) and Tenora & Lusk (1960) and comprehensive analyses of Adenophorea fl ukes and thorny-headed worms were published recently by us Capillariidae gen. sp. (Komorová et al., 2015; Komorová et al., 2016). Host: B. buteo (NIH=10; P=8.4 %; II=1-33; MI=8.5), B. lagopus Comparisons of the fl uke species spectrum in bird orders studied (NIH=1; P=20 %; II=2), A. otus (NIH=5; P=38.5 %; II=3-15; MI=8), within our research showed certain differences between diurnal B. bubo (NIH=1; P=50 %; II=2), S. aluco (NIH=1; P=10 %; II=5), S. (Accipitriformes and Falconiformes) and nocturnal birds of prey uralensis (NIH=4; P=26.7 %; II=2-7; MI=4.25) (Strigiformes). They are similar to fi ndings of Santoro et al. (2012b) Site of infection: small intestine in Calabria (Italy) and Sanmartín et al. (2004) in Galicia (Spain) who observed a relatively narrow range of helminth species within Baruscapillaria falconis (Goeze, 1782) the Strigiformes family, in particular the species specifi c for owls. Host: A. nisus (NIH=1; P=11.1 %; II=6), A. heliaca (NIH=1; This is consistent with our fi ndings in owls with only two detected

318 trematode species (Strigea strigis, Neodiplostomum canalicula- 2000; Borgsteede et al., 2003; Sanmartín et al., 2004; Santoro et tum) as was already published by Komorová et al. (2016). San- al., 2012a, b). Physaloptera alata was the species occurring exclu- toro et al. (2012b) found that the helminth fauna of diurnal birds sively in one species of diurnal raptors. As for the Microtetrameres of prey is much more diverse than nocturnal birds. This distinction , the M. cloacitectus species was confi rmed in diurnal birds could be explained by the fact that the ensemble of diurnal bird of prey and the M. oshmarini species only in the owls. The fi nding species includes hosts with different and varied diet spectrum. In of a belonging to the Tetrameres genus in is consequence, their parasite richness will be the sum of the par- remarkable. It requires more thorough examination based on a ticular fauna of each bird species (e.g. fi sh-eating, insectivores, DNA analysis due to the detection of only a single female indivi- generalist, specialist, etc.) that form the set of hosts. Our results dual of this nematode. The Tetrameres genus is quite common in confi rmed these fi ndings, since among diurnal birds some fl ukes, waterfowls (Sitko & Okulewicz, 2010) but very rare in birds of prey. e.g., Conodiplostomum perlatum, Paracoenogonimus ovatus, and Ferrer et al. (2004) confi rmed Tetrameres sp. in S. aluco in Spain, Metorchis bilis, were detected exclusively in fi sh-eating birds of but the specimen was not determined up to the species level. In prey species, Strigea vandenbrokae was found only in insectivo- Florida, Pence et al. (1975) described the Tetrameres strigiphila rous European honey buzzard, and Parastrigea fl exilis parasitized species from Strix varia, so the species affi liation of the nematode members of the Circus genus. On the other hand, the fl uke S. from Slovakia is highly interesting. The Secernentea class includes falconis has a wide host range among Accipitriformes and Falco- epidemiologically important species and can be considered as the niformes. most pathogenic helminth group in birds of prey. In particular, in- Our results showed that the incidence of fl ukes was the lowest tense infections with species of the Porrocaecum genus identifi ed in the Falconiformes order, where, no species-specifi c parasites in the widest range of hosts represent a serious impact on the were present (Komorová et al., 2016). Only one species of liver health of the birds. It was, for instance, demonstrated by the death fl ukes, M. bilis, detected in our material, was confi rmed also by a of a saker falcon infected with a large number of Porrocaecum DNA analysis (Sitko et al., 2016). angusticolle . Similarly, signifi cant differences in the tapeworm species spectrum Regarding the nematode class of Adenophorea, the Capillariidae in nocturnal and diurnal birds of prey have been revealed. While family was represented most often. These fi ndings were quite diurnal raptors were hosts of several cestode species, such as common and involved a wide range of hosts. However, the spe- Cladotaenia globifera, Cladoteania circi, Cladotaenia spasskii, cies determination was not possible in most cases due to the bad Spiniglans trapezoides, and Mesocestoides perlatus, owls were conservation of materials, except for few specimens that could be parasitized with only two tapeworm species, Paruterina candela- identifi ed, such as Baruscapillaria falconis. braria and Choanotaenia strigium. Among diurnal raptors, the dif- Our results on the species spectrum of acanthocephalans (Palea- ferences between Falconiformes and Accipitriformes orders were canthocephala) in the three orders of birds of prey revealed the also observed. In Accipitriformes, six cestode species were identi- exclusive presence of Centrorhynchus aluconis in Strigiformes, fi ed, whereas in Falconiformes C. globifera was the only identifi ed Centrorhynchus buteonis in Falconiformes, and C. buteonis, or C. tapeworm. Birds of the Accipitriformes order were infected most buteonis. Centrorhynchus globocaudatus co-infections were most frequently and the composition of the tapeworm community was frequently found in Accipitriformes (Komorová et al., 2015, and this the most diverse. This richness could be caused by the diversity of paper). The presence of C. aluconis in diurnal birds of prey was the order that includes species with different trophic habits. It also demonstrated in one case but the parasite reproduction in the host can be associated with a considerable variability of this bird order. was not confi rmed. Among tapeworms, Cladotaenia globifera was the less host-spe- Marked differences in helminth communities between the owls and cifi c species and had the highest prevalence. In contrast, the other the diurnal raptors (Accipitriformes and Falconiformes) have been tapeworms, e.g., C. circi or C. Spasskii, appeared to be specifi c reported by Santoro et al. (2012b) in southern Italy. The majority to their bird hosts. In older papers from the territory of Slovakia, of literature data on acanthocephalans of birds of prey suggests a the synonym Cladotaenia cylindracea was used for the species rather low host specifi city of individual species of the Centrorhy- C. globifera (Ryšavý, 1957; Tenora & Lusk, 1960). In our material, nchus genus. For instance, C. aluconis is considered as an owl fragments of cestodes of the Anoplocephalidae family were detect- parasite in Europe (Kutzer et al., 1982; Kritscher 1985; Ewald & ed in B. buteo. It was probably the only an occasional post-cyclic Crompton, 1993; McInnes et al., 1994; Sitko 1994; Dimitrova et al., transmission from infected small vertebrate prey, being the main 1995; Ferrer et al. 2004; Dimitrova & Dimitrova 2012; Santoro et food component of common buzzards. al., 2012b; Lisitsyna & Greben, 2015), but it has sometimes been Nematodes of the Secernentea class were found in almost all ex- observed also in diurnal raptors (Yamaguti 1963, Illescas Gomez amined species. Parasites of the Cyrnea, Synhimantus and Por- et al. 1993; Borgsteede et al. 2003, Sitko 2011). On the other rocaecum genera infect a broad spectrum of hosts among diurnal hand, C. buteonis has been documented not only in Falconiformes (Falconiformes, Accipitriformes) and also nocturnal (Strigiformes) and Accipitriformes, but also in owls, especially in the Strix genus birds of prey. It was confi rmed also by previous fi ndings (Krone, (Furmaga, 1957; Yamaguti, 1963; Michálek, 1984; Kritscher, 1985;

319 Sitko 2011; Dimitrova & Dimitrova, 2012; Shirazi et al., 2014). The DUBOIS, G. (1970): Synopsis des Strigeidae et des Diplostomatidae widest host range, as confi rmed by the above mentioned authors, (Trematoda). II. Diplostomatidae [Synopsis of the Strigeidae and was observed in C. globocaudatus, primarily infecting diurnal rap- of the Diplostomatidae (Trematoda) II. Diplostomatidae]. Mem. tors (Sanmartín et al., 2004; Lisitsyna & Greben, 2015). Soc. Sci. Nat. Neuchatel, 10: 259 – 727 Within our research, a total of 23 helminth species consisting of EWALD, J.A., CROMPTON, D.W.T. (1993): Centrorhynchus aluconis ten Trematoda species, six Cestoda species, fi ve taxa of the Se- (Acanthocephala) and other helminth species in tawny owls (Strix cernentea class, and one species of Paleacanthocephala were ob- aluco) in Great Britain. J. Parasitol., 79: 952 – 954 served for the fi rst time in birds of prey from Slovakia. Regarding FERRER, D., MOLINA, R., CASTELLA, J., KINSELLA, J.M. (2004): Para- the helminths previously found in Slovakia, lots of new hosts were sitic helminths in the digestive tract of six species of owls (Strigi- listed. The total number of new host observations is 31. Most of formes) in Spain. Vet. J., 167: 181 – 185. DOI: 10.1016/S1090- them were confi rmed for the S. falconis fl uke which was detected 0233(03)00103-5 in eight new avian species. FURMAGA, S. (1957): The helminth fauna of predatory birds (Accip- itres and Striges) of the environment of Lublin. Acta Parasitol., 5: Acknowledgement 215 – 287 GEORGIEV, B.B., BISERKOV, V., GENOV, T. (1986): In toto staining The study was supported by the project “Centre of Excellence for method for cestodes with iron acetocarmine. Helminthologia, 23: Parasitology” (ITMS Code: 26220120022) based on the support 279 – 281 of the Operational Programme “Research & Development” funded GIBBONS, L.M. (2010): Keys to the Nematode Parasites of Ver- from the European Regional Development Fund (1,0). tebrates. Suplementary volume. CAB International, Wallingford (UK), 416 pp. References GIBSON, D.I., JONES, A., BRAY, R.A. (2002): Keys to the Trematoda. Volume 1. CAB International and The Natural History Museum, BARUŠ, V., SERGEEVA, T.P., SONIN, M.D., RYZHIKOV, K.M. (1978): Hel- London, 521 pp. minths of Fish-Eating Birds of the Palearctic Region I. Academia HARTWICH, G. (1975): und Ascaridida. Die Tierwelt Praha, 318 pp. DOI: 10.1007/978-94-009-9972-5 Deutschlands. 62 Teil. Gustav Fischer Verlag, Jena, 256 pp. BORGSTEEDE, F.H.M., OKULEWICZ, A., ZOUN, P.E.F., OKULEWICZ, J. ILLESCAS GOMEZ, M.P., RODRIGUEZ OSORIO, M., ARANDA MAZA, F. (2003): The helminth fauna of birds of prey (Accipitriformes, Fal- (1993): Parasitation of Falconiform, Strigiform and Passeriform coniformes and Strigiformes) in the Nederlands. Acta Parasitol., (Corvidae) birds by helminths in Spain. Res. Rev. Parasitol., 53: 48: 200 – 207 129 – 135 BRAY, R.A., GIBSON, D.I., JONES, A. (2008): Keys to the Trematoda. JOYEUX, CH., BAER, J. G. (1936): Faune de France 30. Cestodes Volume 3. CAB International and The Natural History Museum, [Fauna of France 30. Cestoda]. Typographie Firmin-Didot, 613 pp. London, 805 pp. JOYEUX, CH., TIMON-DAVID, J. (1934): Note sur des Cestodes D´Oi- BUSH, A.O., LAFFERTY, K.D., LOTZ, J.M., SHOSTAK, A.W. (1997): Para- seaux. Récoltés dans la région de Marseille [Note on Cestodes sitology meets ecology on its own terms: Mangolis et al., revisited. of Birds. Collected in the region of Marseille]. Annales du Musée J. Parasitol., 83: 4, 575 – 583. DOI: 10.7939/R3J38KV04 D´Histoire Naturelle de Marseille, Tome XXVI. – Mémoire VI., 5 – 8 DIMITROVA, Z. M., DIMITROVA, N. (2012): Review of species of the KHALIL, L.F., JONES, A., BRAY, R.A. (1994): Keys to the cestode para- phylum Acanthocephala from the Middle-Bulgarian Region. Agric. sites of vertebrates. St Albans, CAB International, 751 pp. Sci. Technol. Stara Zagora, 4: 159 – 165 KOMOROVÁ, P., ŠPAKULOVÁ, M., HURNÍKOVÁ, Z., UHRÍN, M. (2015): Acan- DIMITROVA, Z.M., GIBSON, D.I. (2005): Some species of Centrorhy- thocephalans of the genus Centrorhynchus (Paleacanthocephala: nchus Luhe, 1911 (Acanthocephala: Centrorhynchidae) from the Centrorhynchidae) of birds of prey (Falconiformes) and owls (Stri- collection of the Natural History Museum, London. Syst. Parasitol., giformes) in Slovakia. Parasitol. Res., 114(6): 2273 – 2278. DOI: 62: 117 – 134. DOI: 10.1007/s11230-005-5486-7 10.1007/s00436-015-4420-4 DIMITROVA, Z.M., GEORGIEV, B.B., GENOV, T. (1997): Acanthoce- KOMOROVÁ, P., SITKO, J., ŠPAKULOVÁ, M., HURNÍKOVÁ, Z. (2016): Intesti- phalans of the family Centrorhynchidae (Paleacanthocephala) nal and liver fl ukes of birds of prey (Accipitriformes, Falconiformes, from Bulgaria. Folia Parasitol., 44: 224 – 232 Strigiformes) from Slovakia: uniform of diverse compound? Para- DIMITROVA, Z.M., MURAI, E., GENOV, T. (1995): Some species of the sitol. Res., 115(7): 2837 – 2844. DOI: 10.1007/s00436-016-5034-1 family Centrorhynchidae Van Cleave, 1916 (Acanthocephala) from KOVALIK, P., TOPERCER, J., KARASKA, D., DANKO, Š., ŠRANK, V. (2010): Hungarian birds. Parasit. Hung., 28: 89 – 99 Zoznam vtákov Slovenska k 7. 4. 2010 [The list of birds of Slovakia DUBOIS, G. (1968): Synopsis des Strigeidae et des Diplostomatidae as to 7.4.2010]. Tichodroma, 22: 97 – 10 (In Slovak) (Trematoda). I. Strigeidae [Synopsis of the Strigeidae and of the KRITSCHER, E. (1985): Catalogus faunae Austriae: Aschelminthes, Diplostomatidae (Trematoda). I. Strigeidae]. Mem. Soc. Sci. Nat. Schlauchwürmer; Nemertini, Schnurwürmer. Teil 4. Phylum: Acan- Neuchatel, 10: 1 – 258 thocephala. Verl. Österr. Akad. Wiss. Wien, 4: 1 – 15

320 KRIVJANSKÝ, T. (2009): Sokoliarstvo – 2. diel: Naše dravce a sovy SANTORO, M., KINSELLA, J.M., GALIERO, G., DEGLI UBERTI, B., AZNAR, [Falconry – part 2: Our raptors and owls]. Vydavateľstvo EPOS, F.J. (2012a): Helminth community structure in birds of prey (Accip- 336 pp. (In Slovak) itriformes and Falconiformes) in Southern Italy. J. Parasitol., 98(1): KRONE, O. (2000). Endoparasites of free-ranging birds of prey in 22 – 29. DOI: 10.1645/GE-2924.1 Germany. In: LUMEIJ, J.T., REMPLE, J.D., REDING, P.T., LIERZ, M., SANTORO, M., MATTIUCCI, S., NASCETTI, G., KINSELLA, J.M., DI PRISCO, COOPER, J.E. (Eds) Raptor Biomedicine III. Zoological Educational F., SABATINO, T., D´ALESSIO, N., VENEZIANO, V., AZNAR, F.J. (2012b): Network, pp. 101 – 116 Helminth communities of owls (Strigiformes) indicate strong bi- KUTZER, E., FREY, H., NÖBAUER H. (1982): Zur parasitenfauna öster- ological and ecological differences from birds of prey (Accipitri- reichischer eulenvögel (Strigiformes) [Parasite fauna of Austrian formes and Falconiformes) in Southern Italy. PloS ONE, 7(12), owls (Strigiformes)]. Angew. Parasitol., 23:190 – 197 (In German) e53375. DOI: 10.1371/journal.pone.0053375 LISITSYNA, O.I., GREBEN, O.B. (2015): Acanthocephalans of the SHIRAZI, S., HESARAKI, S., MOSTAFAEI, T.S., DAVOODI, J. (2014): First genus Centrorhynchus (Paleacanthocephala, Centrorhynchidae) report on Centrorhynhus aluconis in common buzzard (Buteo bu- from birds of Ukraine with the description of a new species. Vestn. teo) in Northwest Iran. Acta Vet. (Beogr.), 64: 276 – 280. DOI: Zool., 49(3):195 – 210 10.2478/acve-2014-0026 MCINNES, F.J., CROMPTON, D.W.T., EWALD, J.A. (1994): The distribu- SITKO, J. (1994): Helminths of birds of prey (Falconiformes) and tion of Centrorhynchus aluconis (Acanthocephala) and Porrocae- owls (Strigiformes) in Czech Republic and their infl uence on health cum spirale (Nematoda) in Tawny Owls (Strix aluco) from Great condition of caged birds. Zpr. morav. ornitol. stan., 52: 53 – 84 Britain. J. Raptor Res., 28(1):34 – 38 SITKO, J. (1998): Trematodes of birds of prey of Czech Republic. MEYER, A. (1933): Acanthocephala. Vierter Band, 2. Abt. 2. Buch, Helminthologia, 32: 131 – 146 Leipzig: Academische Verlagsgesellshaft M.B.H., 582 pp. SITKO, J. (2001): Trematodes of owls (Aves: Strigiformes) in the MICHÁLEK, J. (1984): Record of Physaloptera alata Rudolphi, 1819 Czech Republic. Acta Soc. Zool. Bohem., 65: 45 – 56. and Centrorhynchus buteonis (Schrank, 1788) in Falconiformes in SITKO, J. (2011): Checklist of the Acanthocephala in birds in the Czechoslovakia. Folia Parasitol., 31: 383 – 384 Czech Republic and the Slovak Republic. Comenius Museum PENCE, D.B., MOLLHAGEN, T., FORRESTER, D.J. (1975): Tetrameres Přerov, 35 pp. (Gynaecophila) strigiphila sp. n. from the Florida , Strix SITKO, J., OKULEWICZ, A. (2010): Checklist of the Nematodes of birds varia georgica,with Notes on the Status of the Subgenus Gynae- of the Czech Republic and the Slovak Republic. Comenius Muse- cophila (Nematoda: Tetrameridae). J. Parasitol., 61: 494 – 498 um Přerov, 100 pp. PETROCHENKO, V.I. (1958): Acanthocephala of domestic and wild SITKO, J., BIZOS, J., SHERRARD-SMITH, E., STANTON, D.W.G., KOMOR- animals. Vol. II. Moscow, Izdat. AN SSSR, 458 pp. OVÁ, P., HENEBERG, P. (2016): Integrative of European RAUSH, R.L. (1948): Observations on cestodes in North America parasitic fl atworms of the genus Metorchis Looss, 1899 (Tremato- owls with the description of Choanotaenia speotytonis n. sp. (Ces- da: Opisthorchiidae). Parasitol. Int., 65: 258 – 267. DOI: 10.1016/j. toda: Dipylidiinae). Faculty Publications from the Harold W. Manter parint.2016.01.011 Laboratory of Parasitology, 462 – 471 ŠKARDA, J. (1964): The helminthfauna of some wild birds in Czech- RYŠAVÝ, B. (1957): Zur Kenntnis der Helminthenfauna der Vögel oslovakia. Acta Univ. Agric. Brno B, 12: 269 – 293 in der Tsechoslowakei [To the knowledge of the helminthfauna of TENORA, F., LUSK, S. (1960): Beitrag zur näheren Kenntnis der Hel- the birds in Czechoslovakia]. Českoslov. parasit., 4: 299 – 329 (In minthenfauna bei Raubvögeln (Falconiformes) in der Tschecho- German) slowakei [Contribution to the closer knowledge of the helminthfau- SANMARTÍN, M.L., ÁLVAREZ, F., BARREIRO, G., LEIRO, J. (2004): Hel- na in birds of prey (Falconiformes) in Czechoslovakia]. Acta Univ. minth fauna of Falconiform and Strigiform birds of prey in Galicia, Agric. Brno A, 2: 205 – 211 (In German) Northwest Spain. Parasitol. Res., 92: 255 – 263. DOI: 10.1007/ YAMAGUTI, S. (1963): Acanthocephala. Vol. V, Systema Helminthum. s00436-003-1042-z Interscience, New York, 423 pp.

321